Fish protein hydrolysate in diets for Nile tilapia post-larvae

Thiberio Carvalho da Silva(1), Joana D’Arc Mauricio Rocha(1), Pedro Moreira(1), Altevir Signor(1) and Wilson Rogerio Boscolo(1)

(1)Universidade Estadual do Oeste do Paraná, Campus Toledo, Rua da Faculdade, no 2.550, CEP 85903-000 Toledo, PR, Brazil. E-mail: [email protected], [email protected], [email protected], [email protected], [email protected]

Abstract – The objective of this work was to determine the apparent digestibility coefficient (ADC) of crude protein, crude energy, fat, and dry matter of fish protein hydrolysate (FPH), made of by-products of Nile tilapia (Oreochromis niloticus) and whole sardines (Cetengraulis edentulus), and to evaluate the productive performance and muscle fiber growth of Nile tilapia post-larvae. Two trials were conducted, the first one to determine the digestibility in 120 fingerlings (70.0±2.0 g), and the second one to evaluate the productive performance of 375 post-larvae, with three days of age, which were distributed in 25 aquaria with 30 L of useful volume. Five diets were prepared based on vegetable ingredients, to which fish were included at 0, 2, 4, 6, and 8% FPH. For the evaluation of muscle growth, eight fish of each experimental unit were used. The ADC values found were: 98.29% for dry matter; 99.28% for crude protein; and 99.13% for gross energy. The best zootechnical response for the productive performance resulted from the treatment with the inclusion of fish hydrolysate at 4.75%. The diets affected the frequency of the muscle fiber diameters, mainly the growth by hyperplasia. FPH can be efficiently used, and its inclusion at 4.75% is indicated in the diets for Nile tilapia in the post-larvae stage. Index terms: Cetengraulis edentulus, Oreochromis niloticus, digestibility, fish meal, nutrition, peptides, pisciculture. Hidrolisado proteico de peixe em dietas para pós-larvas de tilápia-do-nilo Resumo – O objetivo deste trabalho foi determinar o coeficiente de digestibilidade aparente (CDA) da proteína bruta, da energia bruta, da gordura e da matéria seca de um hidrolisado proteico de peixe (HPP), feito de resíduos de tilápia-do-nilo (Oreochromis niloticus) e sardinha inteira (Cetengraulis edentulus), e avaliar o desempenho produtivo e o crescimento das fibras musculares de pós-larvas de tilápia-do-nilo. Realizaram-se dois ensaios, o primeiro para a determinação da digestibilidade em 120 alevinos (70,0±2,0 g) e, o segundo, para avaliação do desempenho produtivo de 375 pós-larvas, com três dias de idade, distribuídas em 25 aquários (unidade experimental) com volume útil de 30 L. Cinco rações à base de ingredientes vegetais foram elaboradas, às quais se incluíram os peixes a 0, 2, 4, 6 e 8% de HPP. Para a avaliação do crescimento muscular, oito peixes de cada unidade experimental foram utilizados. Os valores de CDA encontrados foram: 98,29% para matéria seca; 99,28% para proteína bruta; e 99,13% para energia bruta. As melhores respostas zootécnicas quanto ao desempenho produtivo resultaram do tratamento com a inclusão do hidrolisado proteico a 4,75%. As dietas influenciaram a frequência do diâmetro das fibras musculares, principalmente o crescimento por hiperplasia. O HPP pode ser eficientemente utilizado, e sua inclusão a 4,75% é indicada em dietas de tilápia-do-nilo na fase de pós-larva. Termos para indexação: Cetengraulis edentulus, Oreochromis niloticus, digestibilidade, farinha de peixe, nutrição, peptídeos, piscicultura.

Introduction To achieve satisfactory performance indices, it is recommended that, in the initial stage, part of the The production of larvae and fry in the quantity and dietary protein be of animal origin because of the quality to meet the growing demand of fish farming better profile of available amino acids and minerals depends on efficient solutions to problems in the (Galdioli et al., 2000; NRC, 2011). Therefore, fish meal rearing process. Feeding outstands as the main factor continues to be the main protein source in diets for among those responsible for failures in larviculture, most species of farmed fish because of the balanced (Phelps, 2010). amino acid profile and the composition of essential

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 486 T.C. da Silva et al.

fatty acids, digestible energy, vitamins, and minerals evaluate the productive performance and muscle fiber (Tacon & Metian, 2008). growth of Nile tilapia post-larvae. However, worldwide fish meal production has staganated by approximately 6–7 million tons in Materials and Methods recent years, and with the increasing demand, its value has increased, raising production costs in aquaculture Digestibility and zootechnical performance trials systems (Tacon & Metian, 2008; Merino et al., 2010). were carried out at the aquaculture and fish nutrition Therefore, several studies have been conducted on laboratory of Grupo de Estudos de Manejo na the total or partial replacement of fish meal in the Aquicultura (Gemaq), of Universidade Estadual do preparation of diets for aquatic organisms, in order Oeste do Paraná (Unioeste), Campus Toledo, in the to maintain the nutritional standards of the feeds municipality of Toledo, PR, Brazil. (Teixeira et al., 2006). The production of FPH consisted of 80% residues An alternative with great potential is the use of by- from Nile tilapia filleting (heads, viscera, scales, fins, products of the fish-processing industry, in the form vertebral column, and adhered tissues) and 20% whole of protein hydrolysate and fish of low-commercial sardine which were used to enhance the aroma and value. The hydrolysis process is defined as the protein taste of FPH, in order to improve the final product breakdown into peptides of various sizes. This attractiveness (Broggi, 2014). This raw material was breakdown can be achieved chemically (with acids or crushed in a CAF food processor , model Boca 5, bases), or biologically (with enzymes). The enzymatic 250-watt power and 30 kg h-1 capacity; then, a water process is more promising, as it generates a product volume equivalent to 20% of the mass value was with high functionality and nutritional value (Naylor added and homogenized. The mixture was placed for et al., 2009; Pasupuleti & Braun, 2010). approximately 5 min in a RW 20 mechanical stirrer The composition of a protein hydrolysate, produced (Ika Brasil Equipamentos Laboratoriais, Analíticos e from fish residue, may contain on average 78.75% Processos Ltda., Campinas, SP, Brazil). Subsequently, crude protein, 3.42% fat, and 12.51% ash (Nilsang et butylated hydroxytoluene (BHT) and butylated al., 2005). The partial replacement of the fish meal hydroxyanisole (BHA) were added at 0.01%. The with this product, even at low percentages, shows a temperature was adjusted to 60°C in a water bath to beneficial effect on the productive performance and promote the enzymatic activity. Alcalase enzyme was immunological activity of several fish species, mainly added at 0.5% and stirred continuously for 60 min. in the early stages of life (Refstie et al., 2004; Hevroy After this time, the enzymatic activity was stopped by et al., 2005). raising the temperature to 85°C for 15 min, and a food Tang et al. (2008) have shown that including up to preservative (citric acid) was added. At the end of the 10% fish protein hydrolysate (FPH) in the diet of yellow process, the liquid hydrolysate was filtered through a croaker (Pseudosciaena crocea) improved the growth 0.5 mm steel sieve to remove small bones. and immunological parameters of this fish. Likewise, To determine digestibility, the diets were elaborated Lian et al. (2005) and Chotikachinda et al. (2013) with an extruded practical feed (used as reference), found positive effects with FPH supplementation in and an extruded test feed composed of 80% of the the diet of the studied species. The results found in reference feed and 20% of the ingredient to be tested, these studies may be related to the high palatability adding 0.1% chromium oxide, used as inert marker of FPH, which contains biologically active, immune- (NRC, 2011) (Table 1). stimulating peptides with antibacterial properties For the feed production, the ingredients were that can be produced during the hydrolysis process initially milled in a hammer-type grinder with a 0.7 (Kotzamanis et al., 2007). mm sieve, and, then, weighed and mixed manually. The objective of this work was to determine the The crushed feed was moistened with 20% water, and apparent digestibility coefficient (ADC) of crude extruded in an ExMicro apparatus (Exteec Máquinas, protein, crude energy, fat, and dry matter of FPH, made Ribeirão Preto, SP, Brazil), with 10 kg h-1 production of by-products of Nile tilapia (Oreochromis niloticus) capacity. After this processing, the feeds were oven and whole sardines (Cetengraulis edentulus), and to dried at 55°C for 12 hours.

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 Fish protein hydrolysate in diets for Nile tilapia 487

Nile tilapia juveniles (120) with a mean mass of CDA(n) = {100 -[100 ×(%Cr2O3d × %Cr2O3f) × (%Nf / 70±2 g were used. Fish were randomly distributed in %Nd)]}, in which: CDA (n) is the nutrient digestibility six 90 L conical tanks suitable for the collection of coefficient; %Cr2O3d is the percentage of chromium feces. The juveniles remained in the tanks for seven oxide in the diet; %Cr2O3f is the percentage of days in the tanks, in order to adapt to the diets and to chromium oxide in feces; %Nf is the percentage of the experimental conditions. The treatments, randomly nutrient in feces; %Nd is the percentage of nutrient in assigned at the beginning of the adaptive period, the diet. And CDA (i) = {CDAdt + [(CDAdt - CDAdr) consisted of three tanks with reference feed, and three × (0.8×Ddr / 0.2×Ding)]}, in which: CDA (i) is the tanks with test feed. Fish were fed at 09:00, 12:00, apparent digestibility coefficient of the ingredient; 0.8 15:00, and 18:00 h. Two hours after the last feeding, the is the percentage of the reference diet; CDAdt is the tanks were cleaned, and 70% of the water volume was apparent digestibility coefficient of the test diet; 0.2 exchanged, to avoid contamination of the feces by feed is the percentage of the ingredient; and CDAdr is the debris. Finally, the collecting cups were attached to the apparent digestibility coefficient of the reference diet. bottom of the tanks and, at 07:00 h of the following The reference feed and the test feed were analyzed day, feces were collected and immediately stored in a for dry matter, ash, crude protein, fat, energy, and - freezer at 15ºC until the start of the analyses. chromium oxide. The following components of the The coefficients of apparent digestibility and gross feces were analyzed: crude protein, gross energy, fat, energy of the nutrients in the diets and FPH were and chromium oxide. The analyses of the diets and calculated according to the NRC equations (2011), feces followed the methodology described by Horwitz adapted for 20% of the feed inclusion, as follows: (2005), except for the chromium analysis that followed the protocol described by Bremer Neto et al. (2003). The zootechnical performance of Nile tilapia post- Table 1. Composition of the reference diet used for larvae was evaluated in 375 three-day-old Nile tilapia determination of the apparent digestibility coefficient post-larvae, which were distributed in 25 aquaria of (ADC) of fish protein hydrolysate (FPH). 30 L useful volume each, in a completely randomized Ingredient Percentage (%) design, with five treatments and five replicates, in Soybean meal 27.51 which the experimental unit consisted of an aquarium Rice meal 25.00 with 15 animals. Each aquarium had its own water Corn grain 17.87 Fish meal 15.00 aeration and heating system. The aquaria were Wheat gluten 8.00 siphoned twice a day: once in the morning and again in Poultry meal 5.00 the late afternoon. Fish were fed at 08:00, 10:00, 12:00, Supplement (mineral + vitamin)(1) 1.00 14:00, and 18:00 h. The experiment lasted 40 days. Salt 0.30 Five feeds were prepared based on ingredients of Chromium oxide 0.10 Antifungal 0.20 plant origin, with five different percentages of FPH: Antioxidant 0.02 0, 2, 4, 6, and 8%. The experimental diets were Total 100.00 formulated according to the NRC recommendation Calculated values (2011) (Table 2). The feeds were extruded according Starch (%) 32.00 to the procedure described for the digestibility trial; Calcium (%) 1.26 DE tilapia (kcal kg-1) 3,118 however, shortly after drying, the feeds were ground Fat (%) 3.12 again to obtain a 0.7 mm feed. Methionine (%) 0.57 At the end of the experimental period, fish were Digestible protein (%) 29.73 fasted for 24 hours, then the individual measurements Threonine (%) 1.19 of mass (g) and total length (cm) were recorded. The (1)Guarantee levels by kilogram of product: 500,000 IU vitamin A; evaluated zootechnical performance variables were: 200,000 IU vitamin D3; 5.000 mg vitamin E; 1,000 mg vitamin K3; 1,500 mg vitamin B1; 1,500 mg vitamin B2; 1,500 mg vitamin B6; 4,000 mg final mass, mass gain, specific growth rate, protein vitamin B12; 15,000 mg vitamin C; 50 mg biotin; 7,000 mg nicotinamide; efficiency rate, survival rate, and batch uniformity. 500 mg folic acid; 4,000 mg calcium pantothenate; 10,000 IU inositol; 40,000 mg choline; 10 mg Co; 500 mg Cu; 5,.000 mg Fe; 50 mg I; 1,500 In both experiments, the water temperature, mgMn; 10 mgSe; and 5,000 mg Zn. dissolved oxygen, and pH were measured daily using a

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 488 T.C. da Silva et al.

HI 9828 multi-parameter (Hanna Instruments Portugal obtained in a microtome and stained with hematoxylin- Ltda., Póvoa de Varzim, Portugal) and remained eosin. Using an image analysis system, morphometry within the recommended amounts for the species was conducted to determine the smallest diameter of cultivation (Ridha & Cruz, 2001). The average values 200 muscle fibers per animal. The data on diameter (D) obtained in the digestibility trial were: temperature, were separated, as described in Assis et al. (2004), into 25.12°C ± 1.15°C; dissolved oxygen, 4.55±0.64 mg L-1; the following classes: c10, D ≤ 10 μm; c20, 10 < D ≤ and pH, 6.68±0.26. The average values obtained 20 μm; c30, 20 < D ≤30 μm; and c40, 30 < D ≤ 40 μm. in the zootechnical performance test were: water On the basis of the results of diameter classification, temperature, 26.26°C±0.50°C; dissolved oxygen, the degree of hypertrophic and hyperplastic growth 5.93±0.34 mg L-1; and pH, 6.23±0.40. of muscle fibers was evaluated according to Alami- In the morphometric analyses of muscle fiber, Durante et al. (2010). eight fish from each experimental unit were used to Data on zootechnical performance and histology evaluate muscle growth. These samples were fixed in were subjected to the analysis of variance, and the means 10% buffered formalin for 24 hours, and processed were compared by the Tukey’s test, at 5% probability. for inclusion in paraffin. Cross sections (5 μm) were The best level of FPH inclusion was determined by a

Table 2. Composition of experimental diets based on plant ingredients with fish protein hydrolysate (FPH) inclusion for post-larvae of Nile tilapia (Oreochromis niloticus).

Ingredient FPH (%) 0 2 4 6 8 Soybean meal 39.79 39.26 39.29 39.19 39.21 Corn gluten 25.10 24.31 23.07 21.12 21.10 Corn grain 12.57 12.89 13.10 13.51 13.13 FPH 0.00 2.00 4.00 6.00 8.00 Rice meal 5.00 5.00 5.00 5.00 5.00 Wheat gluten 5.00 5.00 5.00 5.00 5.00 Dicalcium phosphate 3.85 3.84 3.82 3.81 3.80 Sobean protein isolate 3.00 3.00 3.00 3.00 3.00 Supplement (mineral + vitamin)(1) 1.00 1.00 1.00 1.00 1.00 L-threonine 0.23 0.22 0.22 0.21 0.21 Antifungal 0.20 0.20 0.20 0.20 0.20 Soybean oil 4.07 3.09 2.11 1.13 0.15 Vitamin C 0.10 0.10 0.10 0.10 0.10 L-tryptophan 0.06 0.06 0.05 0.05 0.05 DL-methionine 0.01 0.01 0.02 0.02 0.03 Antioxidant 0.02 0.02 0.02 0.02 0.02 Total 100.00 100.00 100.00 100.00 100.00 Calculated values Linoleic acid (%) 03.12 2.70 2.28 1.86 1.44 Starch (%) 21.40 21.41 21.41 21.41 21.41 Calcium (%) 1.10 1.10 1.10 1.10 1.10 DE tilapia (kcal kg-1) 3,500 3,500 3,500 3,500 3,500 Fat (%) 6.21 6.20 6.19 6.19 6.18 Methionine (%) 0.75 0.75 0.75 0.75 0.75 Digestible protein (%) 41.30 41.30 41.30 41.30 41.30 Threonine (%) 1.70 1.70 1.70 1.70 1.70 Tryptophan 0.43 0.43 0.43 0.43 0.43 (1)Guarantee levels per kilogram of product: 500,000 IU vitamin A; 200,000 IU vitamin D3; 5,000 mg vitamin E; 1,000 mg vitamin K3; 1,500 mg vitamin B1; 1,500 mg vitamin B2; 1,500 mg vitamin B6; 4,000 mg vitamin B12; 15,000 mg vitamin C; 50 mg biotin; 7,000 mg nicotinamide; 500 mg folic acid; 4,000 mg calcium pantothenate; 10,000 IU inositol; 40,000 mg choline; 10 mg Co; 500 mg Cu; 5,000 mg Fe; 50 mg I; 1,500 mg Mn; 10 mg Se; and 5,000 mg Zn.

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 Fish protein hydrolysate in diets for Nile tilapia 489

quadratic equation, associated with the linear response The values of productive performance – final mass, plateau (LRP) model. Data were calculated by the mass gain, specific growth rate, and batch uniformity statistical software SAEG (Universidade Federal de – showed a quadratic effect (p<0.05) with the FPH Viçosa, Viçosa, MG, Brazil). inclusion. However, survival was not affected (p>0.05) by the experimental diets (Table 3). The association of Results and Discussion the quadratic effect with the LRP model was adjusted only for the final mass, mass gain (indicating the same The centesimal composition showed that FPH had value), and specific growth rate, where the maximum 40.74% crude protein, 54.06% lipids, 3.23% ash, and inclusion determined were 4.75 and 4.77%, respectively −1 6.429 kcal kg of gross energy (values based on dry (Figure 1). matter). These values are similar to other hydrolysates mentioned in the literature, produced with fish residues, such as: shrimp, with 46.7% crude protein (Bueno- Solano et al., 2009); tilapia, with 37.7% crude protein (Abdul-Hamid et al., 2002); and croaker, with 47.09% crude protein (Martins et al., 2009). The nature and quality of the raw material are two of the factors that can affect the results obtained from the composition, and that can affect characteristics as the quality and functionality of the final product (Choi et al., 2009). The values for ADCs of crude protein, gross energy, fat, and dry matter were, respectively, 99.28, 99.13, 97.64, and 98.29%. The high-protein digestibility may be associated with the increased solubility, and a structural unfolding of the protein molecule into smaller peptide units occurred during hydrolysis (Van Der Plancken et al., 2003). These smaller molecules, generated by the hydrolysis process, show considerably higher-intestinal absorption kinetics for solutions that contain only dipeptides and tripeptides, or partially hydrolyzed proteins, than those composed only of free amino acids (Fairclough et al., 1980; Zhanghi & Mattews, 2010). The speed of absorption of free amino acids and small peptides is attributed to factors such as competition between amino acids and the transport of amino acids. Free amino acids are rapidly absorbed only in the proximal small intestine, whereas dipeptides and tripeptides are absorbed in both the proximal and distal portions of the small intestine; dipeptides and tripeptides have a faster rate of absorption (Frenhani & Burini, 1999; Ronnestad & Morais, 2008). In vivo digestibility of FPH is still rarely evaluated. However, in vitro digestibility shows slightly lower results than those found in the present study. Hevroy Figure 1. Best fish protein hydrolysate (FPH) inclusion et al. (2005) found 95% dry matter, 98% gross energy, level for final mass (A), mass gain (B), and specific growth and 91% lipids; and Foh et al. (2011) mentioned values rate (C), by means of the first intercept of the quadratic of 93.2% protein digestibility. equation with LRP plateau.

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 490 T.C. da Silva et al.

Earlier studies have shown that diets supplemented of FPH affected the frequency distribution of muscle with FPH can improve the productive performance of fibers (p<0.05), with a higher number of fibers with several fish species in the early stages of life (Kotzamanis a diameter below 10 μm; and the treatment with 2% et al., 2007; Tang et al., 2008; Chotikachinda et al., of FPH resulted in 74.06% fibers in this size class 2013). These findings are corroborated by the data (Table 4). This indicates growth by hyperplasia, obtained in the present study. which is characterized by fiber diameters lower than The main causes of the positive effect of FPH 20 μm (Rowlerson & Veggetti, 2001; Johnston & are associated with improved palatability and Hall, 2004). high digestibility of the protein, which stimulates The process of hyperplasia is predominant in the digestive enzymes and channels nutrients for biomass initial life stages of animals (Almeida et al., 2010); production (Hevroy et al., 2005; Zheng et al., 2013). nevertheless, as indicated in the present study, factors The positive effects on the growth rate and the final such as nutrition may affect the dynamics of muscle mass of salmon juveniles, fed on a diet containing 5 fiber growth. With the increased FPH inclusion to 8% FPH, are mentioned by Berge & Storebakken corresponding to the post-larvae mass gain, there was (1996). Likewise, Zheng et al. (2013) observed that a frequency decrease in the c10 class muscle fiber and flounder fed 3.7% FPH showed a better growth and a consequent increase in the c20 class, that is, there feed efficiency. The inclusion of FPH above 50% may was a negative correlation between mass gain and lead to a decrease of feed intake, which is caused by class <10 (−0.64), and a positive correlation for class a change in the palatability of the hydrolysate due c20 (0.62). In a study conducted with 35-day-old pacu to bitter-tasting peptides or rancid lipid compounds, post-larvae, Leitão et al. (2011) also show the effect of which result in decreased feed consumption and diet on the proportion of muscle fibers in hypertrophy animal growth (Hevroy et al., 2005). The inclusion and hyperplasia.

Table 3. Perfomance of post-larvae of Nile tilapia (Oreochromis niloticus) fed diets with different levels of fish protein hydrolysate (FPH) inclusion.

Variable Fish protein hydrolysate inclusion (%) Coeficient of p-value 0 2 4 6 8 variation (%) Final mass (g)(1) 0.40±0.02 0.44±0.03 0.50±0.03 0.57±0.01 0.52±0.03 18.84 <0.0001** Mass gain (g)(2) 0.39±0.02 0.42±0.03 0.48±0.03 0.56±0.01 0.52±0.03 13.61 <0.0001** Specific growth rate (%)(3) 12.33±0.19 12.63±0.13 12.97±0.23 13.51±0.09 13.21±0.19 3.34 0.0180* Batch uniformity (%)(4) 65.62±3.15 72.54±5.52 77.12±4.34 74.48±2.17 66.62±4.33 8.63 0.0003** Survival (%)(5) 88.33±6.38 83.33±6.66 90.00±11.57 90.00±0.67 86.67±10.88 9.08 0.8385ns (1)Final mass (quadratic effect, FM = -0.024t2 + 0.381t + 0.3933, R2=73). (2)Mass gain (quadratic effect, MG = -0.0024t2 + 0.0381t + 0,3833, R2=0,74). (3)Specific growth rate (quadratic effect, SGR = -0.0188t2 + 0.2791t + 12.279, R2=0,79). (4)Batch uniformity (quadratic effect, BU = -0.6537t2 + 5.1505t + 63.892, R2=52). (5)Survival (no effect). nsNonsignificant. * and **Significant at 5 and 1% probability, respectively.

Table 4. Occurrence frequency of white muscle fibers in diameter classes – c10 (<10), c20 (10–20), c30 (20–30), and c40 (>30) –, in post-larvae of Nile tilapia (Oreochromis niloticus) diets with different levels of fish protein hydrolysate (FPH) inclusion.

Diameter class Fish protein hydrolysate inclusion (%) Coeficient of p-value (µm) 0 2 4 6 8 variation (%) c10 58.25ab 74.06b 68.38ab 60.87ab 51.83a 20.76 0.0225* c20 41.75 25.94 31.56 38.36 44.41 34.99 0.0580ns c30 0.00a 0.00a 0.06a 0.71a 3.34b 76.90 <0.0001** c40 0.00a 0.00a 0.00a 0.06a 0.42a 11.73 0.0002** nsNonsignificant. * and **Significant at 5 and 1% probability, respectively.

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 Fish protein hydrolysate in diets for Nile tilapia 491

Conclusions BUENO-SOLANO, C.; LÓPEZ-CERVANTES, J.; CAMPAS- BAYPOLI, O.N.; LAUTERIO-GARCÍA, R.; ADAN-BANTE, 1. The apparent digestibility of crude protein N.P.; SÁNCHEZ-MACHADO, D.I. Chemical and biological (99.28%), fat (99.13%), dry matter (97.64%), and characteristics of protein hydrolysates from fermented shrimp by- products. Food Chemistry, v.112, p.671-675, 2009. DOI: 10.1016/j. energy utilization (98.29%) show that the fish protein foodchem.2008.06.029. hydrolysate can be used efficiently by Nile tilapia CHOI, Y.J.; HUR, S.; CHOI, B.-D.; KONNO, K.; PARK, J.W. (Oreochromis niloticus). Enzymatic hydrolysis of recovered protein from frozen small 2. The growth of muscle fibers is characterized by croaker and functional properties of its hydrolysates. Journal hyperplasia. of Food Science, v.74, p.C17-C24, 2009. DOI: 10.1111/j.1750- 3. The inclusion of the fish protein hydrolysate 3841.2008.00988.x. at 4.75% is indicated in diets for Nile tilapia, in the CHOTIKACHINDA, R.; TANTIKITTI, C.; BENJAKUL, post‑larval phase. S.; RUSTAD, T.; KUMARNSIT, E. Production of protein hydrolysates from skipjack tuna (Katsuwonus pelamis) viscera as feeding attractants for Asian seabass (Lates calcarifer). Acknowledgments Aquaculture Nutrition, v.19, p.773-784, 2013. DOI: 10.1111/ anu.12024. To Fundação Araucária, for financial support. FAIRCLOUGH, P.D.; HEGARTY, J.E.; SILK, D.B.; CLARK, M.L. Comparison of the absorption of two protein hydrolysates References and their effects on water and electrolyte movements in the human jejunum. Gut, v.21, p.829-834, 1980. ABDUL-HAMID, A.; BAKAR, J.; BEE, G.H. Nutritional quality FOH, M.B.K.; KAMARA, M.T.; AMADOU, I.; FOH, B.M.; of spray dried protein hydrolysate from black tilapia (Oreochromis WENSHUI, X. Chemical and physicochemical properties of mossambicus). Food Chemistry, v.78, p.69-74, 2002. DOI: tilapia (Oreochromis niloticus) fish protein hydrolysate and 10.1016/S0308-8146(01)00380-6. concentrate. International Journal of Biological Chemistry, v.5, p.21-36, 2011. DOI: 10.3923/ijbc.2011.21.36. ALAMI-DURANTE, H.; MÉDALE, F.; CLUZEAUD, M.; KAUSHIK, S.J. Skeletal muscle growth dynamics and expression FRENHANI, P.B.; BURINI, R.C. Mecanismos de ação e controle of related genes in white and red muscles of rainbow trout fed da digestão de proteínas e peptídios em humanos. Arquivos de diets with graded levels of a mixture of plant protein sources as Gastroenterologia, v.36, p.139-147, 1999. substitutes for fishmeal. Aquaculture, v.303, p.50-58, 2010. DOI: GALDIOLI, E.M.; HAYASHI, C.; SOARES, C.M.; FURUYA, 10.1016/j.aquaculture.2010.03.012. W.M.; NAGAE, M.Y. Diferentes fontes protéicas na alimentação ALMEIDA, F.L. de A.; PESSOTTI, N.S.; PINHAL, D.; de alevinos de curimba (Prochilodus lineatus, V.). Acta PADOVANI, C.R.; LEITÃO, N.de J.; CARVALHO, R.F.; Scientiarum, v.22, p.471-477, 2000. DOI: 10.4025/actascibiolsci. MARTINS, C.; PORTELLA, M.C.; DAL PAI-SILVA, M. v22i0.2930. Quantitative expression of myogenic regulatory factors MyoD HEVROY, E.M.; ESPE, M.; WAAGB, R.; SANDNES, K.; RUUD, and myogenin in pacu (Piaractus mesopotamicus) skeletal muscle M.; HEMRE, G.–I. Nutrient utilization in Atlantic salmon (Salmo during growth. Micron, v.41, p.997-1004, 2010. DOI: 10.1016/j. salar L.) fed increased levels of fish protein hydrolysate during micron.2010.06.012. a period of fast growth. Aquaculture Nutrition, v.11, p.301-313, ASSIS, J.M.F. de; CARVALHO, R.F.; BARBOSA, L.; 2005. DOI: 10.1111/j.1365-2095.2005.00357.x. AGOSTINHO, C.A.; DAL PAI-SILVA, M. Effects of incubation HORWITZ, W. (Ed.). Official Methods of Analysis of the AOAC temperature on muscle morphology and growth in the pacu International. 18th ed. Gaithersburg: Association of Official (Piaractus mesopotamicus). Aquaculture, v.237, p.251-267, 2004. Analytical Chemists, 2005. DOI: 10.1016/j.aquaculture.2004.04.022. JOHNSTON, I.A.; HALL, T.E. Mechanisms of muscle BERGE, G.M.; STOREBAKKEN, T. Fish protein hydrolyzate in development and responses to temperature change in fish larvae. starter diets for Atlantic salmon (Salmo salar) fry. Aquaculture, American Fisheries Society Symposium, v.40, p.85-116, 2004. v.145, p.205-212, 1996. DOI: 10.1016/S0044-8486(96)01355-5. KOTZAMANIS, Y.P.; GISBERT, E.; GATESOUPE, F.J.; BREMER NETO, H.; GRANER, C.A.F.; PEZZATO, L.E.; ZAMBONINO INFANTE, J.L.; CAHU, C. Effects of different PADOVANI, C.R.; CANTELMO O.A. Diminuição do teor de dietary levels of fish protein hydrolysates on growth, digestive óxido de crômio (III) usado como marcador externo. Revista enzymes, gut microbiota, and resistance to Vibrio anguillarum in Brasileira de Zootecnia, v.32, p.249-255, 2003. DOI: 10.1590/ European sea bass (Dicentrarchus labrax) larvae. Comparative S1516-35982003000200001. Biochemistry and Physiology. Part A: Molecular and BROGGI, J.A. Hidrolisado proteico de sardinha (Clupeidae) Integrative Physiology, v.147, p.205-214, 2007. DOI: 10.1016/j. como atrativo alimentar para o jundiá (Rhamdia quelen). cbpa.2006.12.037. 2014. 49p. Dissertação (Mestrado) - Universidade do Estado de LEITÃO, N. de J.; DAL PAI-SILVA, M.; ALMEIDA, F.L.A. Santa Catarina, Lages. de; PORTELLA, M.C. The influence of initial feeding

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002 492 T.C. da Silva et al.

on muscle development and growth in pacu Piaractus RIDHA, M.T.; CRUZ, E.M. Effect of biofilter media on mesopotamicus larvae. Aquaculture, v.315, p.78-85, 2011. DOI: water quality and biological performance of the Nile tilápia 10.1016/j.aquaculture.2011.01.006. Oreochromis niloticus L. reared in a simple recirculating system. LIAN, P.Z.; LEE, C.M.; PARK, E. Characterization of squid- Aquacultural Engineering, v.24, p.157-166, 2001. DOI: 10.1016/ processing byproduct hydrolysate and its potential as aquaculture S0144-8609(01)00060-7. feed ingredient. Journal of Agricultural and Food Chemistry, RONNESTAD, I.; MORAIS, S. Digestion. In: FINN, R.N.; v.53, p.5587-5592, 2005. DOI: 10.1021/jf050402w. KAPOOR, B.G. Fish larval physiology. Enfield: Science MARTINS, V.G.; COSTA, J.A.V.; PRENTICE-HERNÁNDEZ, Publishers, 2008. p.201-262. C. Hidrolisado protéico de pescado obtido por vias química ROWLERSON, A.; VEGGETTI, A. Cellular mechanisms of e enzimática a partir de corvina (Micropogonias furnieri). post-embryonic muscle growth in aquaculture species. In: Química Nova, v.32, p.61-66, 2009. DOI: 10.1590/S0100- JOHNSTON, A.I. (Ed.). Muscle development and growth. San 40422009000100012. Diego: Academic Press, 2001. p.101-130. DOI: 10.1016/S1546- MERINO, G.; BARANGE, M.; MULLON, C. Climate variability 5098(01)18006-4. and change scenarios for a marine commodity: modelling small TACON, A.G.J.; METIAN, M. Global overview on the use of fish pelagic fish, fisheries and fishmeal in a globalized market.Journal meal and fish oil in industrially compounded aquafeeds: trends of Marine Systems, v.81, p.196-205, 2010. DOI: 10.1016/j. and future prospects. Aquaculture, v.285, p.146-158, 2008. DOI: jmarsys.2009.12.010. 10.1016/j.aquaculture.2008.08.015. NAYLOR, R.L.; HARDY, R.W.; BUREAU, D.P.; CHIU, A.; TANG, H.; WU, T.; ZHAO, Z.; PAN, X. Effects of fish protein ELLIOTT, M.; FARRELL, A.P.; FORSTER, I.; GATLIN, hydrolysate on growth performance and humoral immune D.M.; GOLDBURG, R.J.; HUA, K.; NICHOLS, P.D. Feeding response in large yellow croaker (Pseudosciaena crocea R.). aquaculture in an era of finite resources. Proceedings of the Journal of Zhejiang University Science B, v.9, p.684-690, 2008. National Academy of Sciences of the United States of America, DOI: 10.1631/jzus.B0820088. v.106, p.15103-15110, 2009. DOI: 10.1073/pnas.0905235106. TEIXEIRA, E. de A.; CREPALDI, D.V.; FARIA, P.M.C.; NILSANG, S.; LERTSIRI, S.; SUPHANTHARIKA, M.; RIBEIRO, L.P.; MELO, D.C.; EULER, A.C.C.; SALIBA, E. ASSAVANIG, A. Optimization of enzymatic hydrolysis of de O.S. Substituição de farinha de peixes em rações para peixes. fish soluble concentrate by commercial proteases. Journal Revista Brasileira de Reprodução Animal, v.30, p.118-125, of Food Engineering, v.70, p.571-578, 2005. DOI: 10.1016/j. 2006. jfoodeng.2004.10.011. VAN DER PLANCKEN, I.; VAN REMOORTERE, M.; NRC. National Research Council. Nutrient requirements of fish INDRAWATI, I.; VAN LOEY, A.; HENDRICKX, M.E. Heat- and shrimp. Washington: National Academies Press, 2011. 379p. induced changes in the susceptibility of egg white proteins to PASUPULETI, V.K.; BRAUN, S. State of the art manufacturing enzymatic hydrolysis: kinetic study. Journal of Agricultural of protein hydrolysates. In: PASUPULETI, V.K.; DEMAIN, and Food Chemistry, v.51, p.3819-3823, 2003. DOI: 10.1021/ A.L. (Ed.). Protein hydrolysates in biotechnology. Dordrecht: jf026019y. Springer, 2010. p.11-32. DOI: 10.1007/978-1-4020-6674-0_2. ZHANGHI, B.M.; MATTHEWS, J.C. Physiological importance PHELPS, R.P. Recent advances in fish hatchery management. and mechanisms of protein hydrolysate absorption. In: Revista Brasileira de Zootecnia, v.39, p.95-101, 2010. DOI: PASUPULETI, V.K.; DEMAIN, A.L. (Ed.). Protein hydrolysates 10.1590/S1516-35982010001300011. in Biotechnology. Dordrecht: Springer, 2010. p.135-177. REFSTIE, S.; OLLI, J.J.; STANDAL, H. Feed intake, growth, ZHENG, K.; LIANG, M.; YAO, H.; WANG, J.; CHANG, Q. Effect and protein utilisation by post-smolt Atlantic salmon (Salmo of size-fractionated fish protein hydrolysate on growth and feed salar) in response to graded levels of fish protein hydrolysate in utilization of turbot (Scophthalmus maximus L.). Aquaculture the diet. Aquaculture, v.239, p.331-349, 2004. DOI: 10.1016/j. Research, v.44, p.895-902, 2013. DOI: 10.1111/j.1365- aquaculture.2004.06.015. 2109.2012.03094.x.

Received on February 26, 2016 and accepted on October 20, 2016

Pesq. agropec. bras., Brasília, v.52, n.7, p.485-492, jul. 2017 DOI: 10.1590/S0100-204X2017000700002